Accepted Manuscript

Edible insects as innovative foods: Nutritional and functional assessments

Seema Patel, Hafiz Ansar Rasul Suleria, Abdur Rauf

PII: S0924-2244(17)30432-6 DOI: https://doi.org/10.1016/j.tifs.2019.02.033 Reference: TIFS 2439

To appear in: Trends in Food Science & Technology

Received Date: 4 July 2017 Revised Date: 14 April 2018 Accepted Date: 6 February 2019

Please cite this article as: Patel, S., Rasul Suleria, H.A., Rauf, A., Edible insects as innovative foods: Nutritional and functional assessments, Trends in Food Science & Technology, https://doi.org/10.1016/ j.tifs.2019.02.033.

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1 Edible insects as innovative foods: Nutritional and functional assessments 2 3 4 5 6 7 1* 2 3 8 Seema Patel , Hafiz Ansar Rasul Suleria , Abdur Rauf 9 10 1Bioinformatics and Medical Informatics Research Center, San Diego State University, 92182, San Diego, CA, USA 11 2UQ School of Medicine, University of Queensland, Brisbane, QLD 4072, Australia 12 3Department of Chemistry, University of Swabi, Anbar-23561, Khyber Pakhtunkhwa, Pakistan 13 14 15 16 17 18 19 20 21 22 Short running title: Edible insects as dietary components 23 24 Key words: Edible insects; Sustainable food; Protein; Allergen; Cultural taboo 25 26 27 28 29 30 MANUSCRIPT 31 32 33 34 35 36 *Corresponding author and address for correspondence: 37 38 39 Dr. Seema Patel 40 Bioinformatics and Medical Informatics Research Center 41 San Diego State University 42 5500 Campanile Dr San Diego, CA 92182 43 Email: [email protected] 44 45 Dr. Abdur Rauf 46 Department of Chemistry University of Swabi, 47 KPK, Pakistan 48 E-mail:[email protected] 49 ACCEPTED 50 51

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54 Abstract

55 In the face of rising population, food insecurity is emerging as a global challenge. Nutritious sources of food

56 are frantically being searched for. Underutilized food candidates are being assessed for feeding the global

57 population. In this regard, Arthropods, the largest phylum fits the bill, and holds tremendous promise, without

58 harming the environment. Loaded in proteins, fat and minerals, the “edible insects” can alleviate hunger and

59 malnutrition. In fact, in every country, entomophagy is practiced, though mostly among the low-income groups.

60 However, few hiccups lie in the path of their popularization. Their allergenic tissues and pathogen-carrying traits

61 impose threats to human health. Further, the aversion of the Western world towards the insects as a food article

62 impedes their recognition as food. While some crustaceans as shrimp, lobsters, crabs, and krill are gourmet food

63 articles, with high demand, the logicality of neglecting insects as likely food commodities appear to be a

64 psychological perception. Researchers and global regulatory bodies are encouraging further investigations and

65 inclusion of the edible-grade insects to diet. As this movement is at the early stages and given due impetus, it can

66 play significant role in quenching world hunger and reducing the usage of lethal pesticides, this review has been

67 woven around the objective of ‘insects as human food’. 68 MANUSCRIPT 69 70

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77 Introduction

78 As world population surges ahead, food security becomes a gigantic challenge. Hunger and malnutrition is a

79 perpetual problem of poverty-stricken regions. As nutritional deficiency is the root cause of numerous other

80 pathologies, ensuring adequate nourishment for all, is an urgent need. In this regard, arthropods especially edible

81 insects as a protein source is being mulled (Nadeau, Nadeau, Franklin, & Dunkel, 2015; Arnold van Huis et al.,

82 2015). Some arthropods members, especially the crustaceans, are not only food, but are expensive delicacies. Crabs,

83 lobsters, prawns, and shrimps are farmed and exported for their overwhelming demands (Hadley, 2006). The marine

84 crustacean krill (Euphausia superba ) oil is emerging as a pharmaceutical agent and a substitute of fish oil, owing to

85 its high omega-3 fatty acids, choline and antioxidant astaxanthin contents (Barros, Poppe, & Bondan, 2014; Maki et

86 al., 2009). Bee ( Apis sp.)-regurgitated honey, pollen and propolis are expensive dietary supplements (Al-Hariri,

87 2011; Patel, 2016a; Rossano et al., 2012; Silva-Carvalho et al., 2014). Fried honey bees are deemed a delicacy in

88 parts of China. Fig. 1A shows a beehive on a tree. Apiculture is a popular livelihood practice. The scaly cochineal

89 insects ( Dactylopius coccus ) growing on prickly pear cacti are the source of red dye carmine, used in wide array of

90 food products including yoghurts, candies, cupcakes, coffees (Voltolini, Pellegrini, Contatore, Bignardi, & Minale, 91 2014). The pigment carminic acid is the source of the red dye.MANUSCRIPT In countries like Mexico, these insects are farmed (De 92 León-Rodríguez, González-Hernández, Barba de la Rosa, Escalante-Minakata, & López, 2006; Ramos-Elorduy et 93 al., 2011).

94 Other arthropods are not as mainstream food items, though they have been significant part of diet across

95 different cultures. Entomophagy is practiced in countries spanning almost all continents (Raubenheimer & Rothman,

96 2013). The eggs, larvae, pupae, and adults of several arthropods, especially edible insects, are consumed in different

97 forms. Ethnic groups have been consuming them since ages.

98 Apart from the nutritional benefits of edible arthropods, especially edible insects, consumption, they have

99 suddenly caught the attention of food development and regulation bodies for other potent reasons. It is unanimously

100 agreed that edible insects can provide ecological and economic advantages as well. These edible insects can be a

101 cheaper substitute ofACCEPTED the expensive animal proteins. It can bolster the fragile food supply. Edible insects farming can

102 reduce the pressure from agriculture, aquaculture and animal husbandry, by requiring less turnover time, land, water

103 or feed (Premalatha, Abbasi, Abbasi, & Abbasi, 2011). Also, consumption the arthropod/edible insects, which are

104 the major agricultural pests, can lead to low usage of pesticides. These chemicals are polluting the environment,

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105 triggering a wide array of human illnesses. So, eradicating the pests by ingesting them, appears to be a very

106 promising solution. This new energy-efficient, sustainable way of growing food is exciting but beset with pragmatic

107 issues such as pathogenic microorganisms, anti-nutritional factors, allergenicity, and most importantly consumer

108 distaste. Hence, this review discusses the possibilities and pitfalls of 'edible insect as future human food'.

109 Arthropods/edible insects as dietary component across the globe

110 Literature search reveals that consuming arthropods/edible insects is not unique to a geographical region

111 but is a pervasive practice. Almost all Native American and Latin American tribes subsisted on insects (Navarro,

112 Prado, Cárdenas, Santos, & Caramelli, 2010). Kutzadika people inhabiting the Mono Lake region of California ate

113 kutzavi, the alkali fly (Ephydra hians ) pupae (Fig 1D). One variation of the preparation was named ‘cuchaba’. The

114 Maidu people (Digger Indians) of Northern California consumed jet-black carpenter ants ( Camponotus spp.). Paiute

115 Indians inhabiting California's Owens Valley consumed Pandora moth ( Coloradia pandora ) larvae. Mealy plum

116 aphid ( Hyalopterus pruni )-exuded honeydew was harvested by some Native Indian tribes for usage as sugar.

117 Mormon cricket ( Anabrus simplex ), a crop-destroying katydid swarm was another food item for people in Midwest

118 of the USA. In countries like Thailand, and Cambodia, they relish arthropods like grasshoppers, crickets, ants, 119 bamboo borers (Omphisa fuscidentalis ), palm weevil larvae,MANUSCRIPT and scorpions (Hanboonsong, Jamjanya, & Durst, 120 2013). Fig. 1E and 1F shows crickets and grasshoppers on garden plants. In Bangkok, these insects are sold in 121 markets which travelers try as exotic foods. Spiders are relished by some in Vietnam. In Laos, several ethnic groups

122 consume weaver ant eggs, bamboo worms, crickets, and wasps (Barennes, Phimmasane, & Rajaonarivo, 2015). In

123 India, red ants, hornets, and termites are consumed by some tribes. Red weaver ant ( Oecophylla smaragdina )

124 chutney (a condiment), known as ‘chapura’ is a delicacy among tribal in Central India. Fig. 1B shows the ants on a

125 tree. In North East India hornet (Vespa sp.) grubs are consumed. In Arunachal Pradesh, tribal like Nyishi, Galo,

126 Nocte, Shingpo, Tangsa, Deori and Chakma of Arunachal Pradesh consume many insects from Coleoptera,

127 Orthoptera, Hemiptera, Hymenoptera, Lepidoptera, Isoptera, Ephemeroptera, Odonata and Mantodea orders

128 (Chakravorty, Ghosh, & Meyer-Rochow, 2011, 2013). Common red tree dwelling weaver ant (Oecophylla

129 smaragdina ) and termitesACCEPTED (Odontotermes sp.) consumed by the tribals were found to be nutrient-dense (Chakravorty,

130 Ghosh, Megu, Jung, & Meyer-Rochow, 2016). Chapulines, the grasshoppers ( Sphenarium sp.) are relished in parts

131 of Mexico and Central America (Handley et al., 2007). Even, these fried insects are sold as snacks. Other insect

132 genera to be of food importance in Mexico include Phassus, nopal worm ( Laniifera cyclades ), Latebraria

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133 amphipyroides , Arsenura armada , and Spodoptera spp. (Ramos-Elorduy et al., 2011). Mezcal, a distilled alcoholic

134 beverage made from the maguey plant ( Agave americana ) is served with a larva of a moth tequila worm ( Hypopta

135 agavis ) (De León-Rodríguez et al., 2006). A survey of locals in Bondo district of Kenya revealed that they consume

136 onyoso mammon (ant), oyala (termite), ogawo (termite), agaor (termite), and onjiri mammon (cricket). These insects

137 had good quantity of iron (18 to 1562 mg/100), zinc (8 to 25 mg/100 g) and calcium (33 to 341 mg/100 g), the often

138 deficient nutrients in this region (Christensen et al., 2006). An emperor moth ( Gonimbrasia belina ) caterpillar,

139 known as the mopane worm is consumed in Southern Africa (Okezie, Kgomotso, & Letswiti, 2010). African palm

140 weevil ( Rhychophorus phoenicis ) larvae are consumed by some tribes. Biochemical assays of the deffated larvae

141 revealed the composition to be of 66.3% protein, 1,025 mg/100 g potassium and 685 mg/100 g phosphorus (Elemo,

142 Elemo, Makinde, & Erukainure, 2011). The Azande and Mangbetu people of Congo relish the termites or ‘white

143 ants’ (Arnold van Huis, 2017). The Pangwe people in Guinea, Gabon, and Cameroon gather aquatic larvae of dragon

144 flies. In Nigeria, a termite species Macrotermes natalensis , African cricket, Brachytrupes membranaceus , and pallid

145 emperor moth Cirina forda are popular insect foods (Agbidye, Ofuya, & Akindele, 2009). In Carnia region of Italy,

146 moths of the Zygaenidae family, such as Zygaena are eaten as seasonal delicacy. Among European countries, the 147 Netherlands is open to the integration of insects in food (House,MANUSCRIPT 2016). Australian Aborigines traditionally subsisted 148 on Bogong moth ( Agrotis infusa ), larvae of cossid moth ( Xyleutes leucomochla ), and honeypot ant ( Melophorus 149 bagoti Lubbock and Campanoyus spp.) (Warrant et al., 2016). The leafcutter ant (Atta laevigata , Atta cephalotes ,

150 and Atta sexdens ) is eaten in parts of Colombia and Brazil. The adult beetle (Holotrichia parallela Motschulsky) is

151 traditionally consumed in China. On nutritional analysis, the beetle tissue was found rich in protein (70%) and

152 minerals (Yang et al., 2014). Traditional Chinese Medicine (TCM) formulations include cicada chitin (Seabrooks &

153 Hu, 2017). As per a study, hundreds of insect species spanning 96 genera, 53 families and 11 orders, which

154 encompass eggs, larvae, pupae and adults, are consumed in China, by frying, stewing, boiling and braising (Chen,

155 Feng, & Chen, 2009). In Japanese culture, many insects are relished and even served in restaurants. Some popular

156 once include hachinoko (boiled wasp larvae), sangi (fried silk moth pupae) and zazamushi (aquatic insect larvae),

157 semi (fried cicada) andACCEPTED inago (fried grasshopper) (Césard, Komatsu, & Iwata, 2015). Casu Marzu (putrid cheese), a

158 traditional Sardinian sheep milk cheese, as its name suggests includes maggots containing live larvae of cheese fly

159 (Piophila casei ), a part of the cheese fermentation process. This cheese has been found very rich in bioactive

160 compounds γ-aminobutyric acid (GABA) (Manca et al., 2015). Acorns from a variety of oak trees are consumed as

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161 flour, after leaching the tannin part out. Some of the acorns are inhabited by the larvae of acorn weevils ( Curculio

162 sp.). These larvae arerich in fat and protein, which foragers consume. Insects induce gall formation in leaves of

163 several plants. Leaf galls are induced in zebrawood ( Pistacia integerrima ) by chalcidoid wasps (Samra, Ghanim,

164 Protasov, Branco, & Mendel, 2015). These galls have folkloric usage as asthma, diarrhea, psoriasis, fever, liver

165 disorders therapeutics, among others (Uddin, Rauf, Al-Othman, et al., 2012; Uddin, Rauf, Arfan, et al., 2012; Ullah

166 et al., 2014). Abundance of monoterpenes in the galls offer antimicrobial effects (Gerchman & Inbar, 2011; Rand,

167 Bar, Ben-Ari, Lewinsohn, & Inbar, 2014). Fig. 1C shows galls in oak trees. Even stink insects (Hemiptera order) are

168 consumed. The taste of the insects varies depending on the biochemical composition and preparation process. The

169 processing ways of the edible insects for eating purposes include drying, smoking, steaming, blanching, roasting,

170 and cooking (Chen et al., 2009). The consumers describe the foods to vary in taste from mushy, soft, to crispy,

171 crunchy. The flavors have been described as chicken-like, herring-like, almond-like, potato-like etc. Honey, cake,

172 beverage flavoring, drinks among other usages of insects have been documented. The consumption of edible insects

173 in various forms far exceed the meager published literature. The information presented here are just a miniscule

174 fraction of the edible insects in nourishing human throughout the course of evolution. Books can be referred to for 175 further information on ethnic food habits encompassing insectsMANUSCRIPT (Bodenheimer, 1951; Costa-Neto & Dunkel, 2016). 176 With the availability of other food sources, arthropods/edible insects disappeared from the food platter. Fig. 1 shows 177 some edible insects (A ) Honey-containing beehive on a fig tree (B) Red ants on mango tree bark (C) Wasp galls on

178 scrub oak tree (D) Alkali flies on the shore of Mono lake (E) Cricket on lily plant (F) Juvenile grasshopper on

179 hibiscus plants.

180 As nutritious food availability becomes increasingly difficult, Food and Agriculture Organization (FAO) is

181 planning and suggesting the consumption of insects (Nowak, Persijn, Rittenschober, & Charrondiere, 2016).

182 European Commission (EC) is also considering its increased usage in food. These endorsements are supported due to

183 the high protein, micronutrients, and 'feed conversion ratio' of the edible insects (Nowak et al., 2016). Though the

184 wriggling caterpillars or filthy-looking adult arthropods/edible insects do not appear as food in first glance, human

185 diet is all about learnedACCEPTED food practices and acquired tastes. These aspects have been discussed later in details.

186 Inherent risks of entomophagy

187 Among issues that mar the food potential of arthropods/edible insects, their allergenicity and pathogenicity

188 risks are worth-assessing. House dust mites ( Dermatophagoides pteronyssinus ), cockroaches ( Blatella germanica ,

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189 Periplaneta americana ), bees, crustaceans, and moths have large repertoires of allergens that provoke IgE-mediated

190 hypersensitivity in predisposed individuals (Arlian, 2002; Kim & Hong, 2007; Okezie et al., 2010). Insect allergy

191 has been a major cause of occupational health problem. Systemic allergic reactions in beekeepers has been

192 documented (Ludman & Boyle, 2015). These allergens belongs to the biochemical class of serine proteases (trypsin,

193 chymotrypsin, collagenase) (Dumez et al., 2014; Sudha, Arora, Gaur, Pasha, & Singh, 2008; H Wan et al., 2001),

194 aspartic protease, chitinases, calycin, troponin, tropomyosin, arylophorin, glutathione-S-transferase, and chitin

195 (Arlian, 2002; Hindley et al., 2006; Jeong, Hong, & Yong, 2006; Kim & Hong, 2007; Reese, Ayuso, & Lehrer,

196 1999). These allergens disrupt cell membranes, cleave tight junction proteins (occludins) between epithelial cells,

197 induce cytokine proliferation, and provoke immune cell infiltration, among an array of other immune manipulations

198 (Chapman, Wünschmann, & Pomés, 2007; Kempkes, Buddenkotte, Cevikbas, Buhl, & Steinhoff, 2014; Zhang,

199 Zeng, & He, 2014). Chitin, the arthropod exoskeleton is known to trigger tissue inflammation by activating the

200 expression of host chitinases (Da Silva, Pochard, Lee, & Elias, 2010; Wang et al., 2013). Asthma, dermatitis,

201 urticaria, sinusitis, rhinitis, otitis etc. result from the exposure to these allergens (Arshad, 2010). Some of the

202 allergens are capable of causing anaphylaxis as well (Ahmed, Minhas, Namood-E-Sahar, Aftab, & Khan, 2010; 203 Asokananthan et al., 2002; Ichikawa et al., 2009; Macan, Plavec,MANUSCRIPT Kanceljak, & Milkovic-Kraus, 2003). This severe 204 allergy is the resultant of the manipulation of human cytoskeletal elements like actin which controls autophagy, 205 endocytosis, endosomal maturation, among other critical functions (Navarro-Garcia, Sonnested, & Teter, 2010).

206 Scorpion and spider venoms are chymotrypsin-like serine proteases that can cause skin necrosis, human blood

207 coagulation and death (Devaraja, Nagaraju, Mahadeswaraswamy, Girish, & Kemparaju, 2008; Louati, Zouari,

208 Miled, & Gargouri, 2011; Veiga et al., 2000). The allergens arginine kinase, glyceraldehyde 3-phosphate

209 dehydrogenase hemocyanin were detected in Macrobrachium rosenbergii (giant freshwater prawn) while the

210 allergen hexamerin1B was detected in Gryllus bimaculatus (field cricket) (Srinroch, Srisomsap,

211 Chokchaichamnankit, Punyarit, & Phiriyangkul, 2015). Arthropod body fluids also have protease inhibitors,

212 belonging to β-barrel fold, knottins, and Bowman–Birk family. Knottins exist as antimicrobial proteins in plants,

213 some examples beingACCEPTED thionins (Taveira et al., 2016), defensins (Ermakova et al., 2016; Tantong et al., 2016),

214 cyclotides, 2S albumin-like proteins, lipid transfer proteins (LTPs), and knottin-peptides (Nguyen et al., 2015). A

215 conserved domain in this protein topology include a cysteine-rich domain Knot1, which occurs in arthropod

216 defensins (Gracy et al., 2008). The arthropod protease inhibitors can be of Kazal-type (termite) (Ohmuraya &

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217 Yamamura, 2011) or Kunitz-type (spider, tick) (Chmelar, Calvo, Pedra, Francischetti, & Kotsyfakis, 2012; Liu et al.,

218 2015). These inhibitors are capable of blocking human chymotrypsin, elastase, and plasmin (Negulescu et al., 2015;

219 Hu Wan et al., 2013). Some moths and butterflies contain toxic hydrogen cyanide in their tissues, as result of feeding

220 on cyanogenic plants. Burnet moths ( Zygaena filipendulae ) are one of such insects that can metabolize cyanogenic

221 glucosides linamarin and lotaustralin from the Fabaceae family plants (Zagrobelny & Møller, 2011). Monarch

222 butterfly ( Danaus plexippus ) larvae feed on common milkweed ( Asclepias syriaca L.), which causes the

223 accumulation of plant cardenolide in the butterflies (Petschenka & Agrawal, 2015). As cardenolide is a type of

224 cardiac glycoside, birds avoid devouring on these butterflies. So, if human consumes these butterflies, they are likely

225 to be harmful, by meddling with sodium-potassium pumps (Na +/K +-ATPase) (Ogawa, Shinoda, Cornelius, &

226 Toyoshima, 2009).

227 As all organic material are susceptible to pathogenic contamination, the microbial analysis of the food item is

228 required. Improper handling and rearing of arthropods might increase the chance of contracting the infections.

229 Several arthropods/edible insects carry pathogenic viruses (Campos, Bandeira, & Sardi, 2015), bacteria (Hager et al.,

230 2006), protozoa (Takeo et al., 2009), fungi, and nematodes. Arthropods are vectors for a large number of zoonotic 231 diseases such as malaria, Lyme disease. Also, insects are parasitizeMANUSCRIPTd by fungi, exposure to the mycotoxins of which 232 can be perilous for human health. The in silico analysis of cockroach allergens showed the phylogenetic 233 conservation of the quintessential virus, and bacteria virulence domains such as AAA, BRLZ, BTAD, ChtBD3,

234 HALZ, HAMP, HELICc, Hr1, LRRCT, RAB, RUN, Tryp_SPc, WR1, VKc, and VWC among others (Patel, 2016b).

235 Details on these pathogenesis-mediating protein domains can be obtained from SMART (Simple Modular

236 Architecture Research Tool) website (Ponting, Schultz, Milpetz, & Bork, 1999). In this regard, various forms of

237 insect products were analyzed. The dried and powdered forms had higher counts of microbes than the deep-fried,

238 spiced and cooked ones. The dried products had coliforms, Serratia liquefaciens , Listeria ivanovii , Mucor spp.,

239 Aspergillus spp., Penicillium spp., and Cryptococcus neoformans (Grabowski & Klein, 2016). Another heating step

240 of these products might fix the pathogenesis risk. Chapuline consumption has been associated with lead poisoning

241 (Handley et al., 2007).ACCEPTED

242 Fig. 2 presents some nutrients, allergens and anti-nutrients in arthropods. Attractive nutritional composition

243 of a food commodity is not enough if they lack in safety. So, the complete risk assessment of the edible insects-

244 based food candidate must be carried out, before recommending for food (Grabowski & Klein, 2016). As the

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245 inclusion of insects in food platter increases, EU edible insect food safety guide has been published (Robinson,

246 2015).

247 Current scenario and scopes of entomophagy

248 This section presents the current state of entomophagy, undergoing research efforts, and scopes ahead.

249 Mealworms, the larvae of the mealworm beetle ( Tenebrio molitor ) are some of the top suggested insects of food

250 candidature (Nowak et al., 2016). These insects are reported to be high in protein, polyunsaturated fats, and minerals

251 (copper, sodium, potassium, iron, zinc and selenium). This Coleoptera beetle could be bred on bocaiuva ( Acrocomia

252 aculeata) pulp flour (Alves, Sanjinez-Argandoña, Linzmeier, Cardoso, & Macedo, 2016). The larva of the coconut

253 borer ( Pachymerus nucleorum ) could also be grown on the bocaiuva fruit kernel (Alves, Sanjinez Argandoña,

254 Linzmeier, Cardoso, & Macedo, 2016). Among other insect candidates, common housefly (Musca domestica ), the

255 black soldier fly ( Hermetia illucens ), locusts ( Locusta migratoria, Schistocerca gregaria, Oxya spec ., Pachytylus

256 migratorius etc.) and silkworms ( Bombyx mori ) are prominent. This standing arises from their biomass, and amino

257 acid composition (Stamer, 2015). Housefly and black soldier fly, for their interesting nutritional composition were

258 suggested promising for feline and canine foods (Bosch, Zhang, Oonincx, & Hendriks, 2014). 259 Going by the published literature, the topic of ‘arthropods/edibleMANUSCRIPT insects as food candidate’ has garnered huge 260 amount of attention in the past few years. Surveys, panel tests, food fests, and symposiums have led to immense 261 insights. Arthropods especially some of the edible insects are consumed by billions of people worldwide, mostly in

262 low-income countries. The need to supplement their low-nutrient diet has led to the inclusion of the insects, since

263 ages. Like most habits, it has become inherent part of their subsistence now. Western world has access to other

264 sources of nutrients, so entomophagy is rather new to them. Though lobsters, shrimp, crayfish, crabs are relished.

265 Based on the research findings, it is agreed that revulsion towards the edible insects-based food is the result of

266 mindset. Disgust, a psychological conditioning, rejects the creepy-crawlies as edibles (Hamerman, 2016; Menozzi,

267 Sogari, Veneziani, Simoni, & Mora, 2017). Food neophobia, the tendency to decline novel or unknown foods is a

268 common human trait (Demattè, Endrizzi, & Gasperi, 2014). Arthropod especially edible insects based-food

269 neophobia is particularlyACCEPTED high (Caparros Megido et al., 2016). Females were particularly averse towards the insect-

270 based food (Caparros Megido et al., 2016). They preferred beef burgers over insect burgers (Caparros Megido et al.,

271 2016). Masking the gross looks or promoting in a appealing name has often improved the acceptance of a food by

272 the consumers. Incorporation of the minced insects into ready-to-eat preparations and frequent exposure in the form

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273 of food fests etc. is suggested as steps to reduce the repulsion (Caparros Megido et al., 2016). Another study also

274 reports that communicating with potential consumers regarding the environmental benefits of eating edible insects

275 products positively modulates their ingestion propensity (Verneau et al., 2016). Educational campaigns can prime

276 people for adopting entomophagy and can help them overcome their repulsion (Costa-Neto & Dunkel, 2016;

277 Hamerman, 2016). Some researchers suggest the name ‘Shrimp of the land’ for some insects, as a way to make them

278 appear appetizing. Usage of the terms ‘novelty foods’, ‘super foods’, ‘low carbon footprints’ might be catalyst in

279 gaining public approval as well. Many of the abhorred foods of the past are expensive, popular specialty foods now,

280 such as truffles (Patel, 2012a), huitlacoche (Patel, 2016c), quinoa (Maradini Filho et al., 2015), seaweeds (Patel,

281 2012b), krill oil (Tandy et al., 2009), among others. The French are known to relish frog legs, and snake wine is

282 popular in several South Asian countries.

283 Another big hurdle in popularity of insect-based foods is their standing as culturally-inappropriate (Tan,

284 Fischer, van Trijp, & Stieger, 2016). Many religions insist on ‘kosher’, ‘halal’, ‘vegan’ (Costa-Neto & Dunkel, 2016;

285 Fischer, 2008), and these creatures do not fall in that groups. The judgments towards the insect-based foods are made

286 based on these rules as well as conventional eating habits (Tan et al., 2015). Beyond sensory liking, a broader 287 mindset is needed to accept the edible insects as food (Tan etMANUSCRIPT al., 2016). A study based the reaction of Chinese and 288 German testers to cricket-based food was conducted. For their cultural habits, the Chinese testers were open to the 289 products, while the Germans were less willing to try. However, it was found that adequate processing of the insects

290 encouraged their eating (Hartmann, Shi, Giusto, & Siegrist, 2015). In a blind sample tasting encompassing 97 young

291 adults, insect burger received similar response as plant-based burgers (Schouteten et al., 2016). Another study based

292 on cricket-based snacks reflected that the degree of processing influenced the willingness to consume them. The

293 testers preferred the flour and bits of the insect-based snacks than the products mixed with other ingredients (Gmuer,

294 Nuessli Guth, Hartmann, & Siegrist, 2016). Based on the finding, the researchers suggested that the establishments

295 promoting insect-based food ought to attempt to understand the consumer psychology, preferences and modulate

296 their preparation strategies accordingly (Gmuer et al., 2016). For increasing consumer appeal, innovative

297 developments of insect-basedACCEPTED foods are suggested essential by researchers (Shelomi, 2015). In an exposition in

298 Milan, Italy in 2015, the attitudes of various countries on insect-based foods was presented (Shelomi, 2016). While

299 Angola (Africa) showcased certain insects as part of their traditional cuisine, European countries like Belgium and

300 the Netherlands presented their vision of insect-based food development (Shelomi, 2016). Legislatives supporting

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301 them as edible and nutritious can play a big role in their wider popularity (Van Huis & Dunkel, 2017). In fact, a

302 survey of consumers in Kenya, regarding termite-based food products, received a better affirmative response, when

303 the product was recommended by officials (Alemu, Olsen, Vedel, Pambo, & Owino, 2017). Many startups, even in

304 Western world such as California (USA), British Columbia (Canada), are offering edible insect-based food products.

305 Increasing number researchers are optimistic regarding the potential of insects as a sustainable food source

306 (Sun-Waterhouse et al., 2016). The generation of insect-based protein powder is predicted to be environmentally

307 beneficial than convention protein-rich food products (Smetana, Palanisamy, Mathys, & Heinz, 2016). For

308 sustainable production of the arthropods especially edible insects, rearing and harvesting is crucial (Costa-Neto &

309 Dunkel, 2016). Thailand is at the forefront of farming food-grade insects, such as crickets and palm weevils

310 (Hanboonsong et al., 2013), while countries like the Netherlands are following suit. As per an article, by 2014,

311 edible insect business has already swelled into a $20 million industry (Hoffman, 2014). Yet, entomo-culture is a new

312 area, and need to be researched. Mass-rearing, and post-harvest technologies need to be developed (Rumpold &

313 Schlüter, 2013). Given the low cost involved in the insect farming, it can be a livelihood opportunity for people in

314 low-economy regions. Entomo-culturing and entomophagy even falls within the scope of 'One World - One Health' 315 (OWOH) movement (Yates-Doerr, 2015). This movement MANUSCRIPTencourages collaborations to mitigate global threats 316 (Gibbs and Anderson 2009).

317 Relevance of entomophagy

318 Many of the arthropod ingestion habit started to get rid of the nuisance insects or plantation pests, such as the

319 red ants, grasshoppers, and locusts. Also, during the hunter-gatherer phase of evolution, human did not have much

320 choice of food, unlike now. Starved of food, they had developed the habit to supplement their food with locally- and

321 seasonally-available insects. Over a long period of time, they acquired a taste for them. Even today, iron-deficient

322 individuals suffering from a condition ‘pica’ eat insects, among other random, non-food things (Advani, Kochhar,

323 Chachra, & Dhawan, 2014). The above fact has been mentioned to relate that in the past, before agriculture and

324 industrialization, when food was in scanty, hunger forced mankind to feed on diverse nutritional sources. However,

325 with the progress of ACCEPTEDcivilization ample food options led to the decline in entomophagy practice.

326 Like most problems in science, entomophagy is a novel idea with pros and cons. While several of them are

327 good sources of nutrition, especially proteins, they are endowed with health risks too. Most of them have chitin and

328 human cytoskeleton-manipulating enzymes. May be proper cooking techniques can deactivate the allergenic

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329 proteins. Still individuals atopic to them ought to avoid them. People tolerant to the arthropods especially edible

330 insects can benefit from them as a source of nutrition. Entomophagy can rise in popularity, if comparative studies on

331 the nutritional value of food-grade edible insects and other nutritious food sources, such as animal proteins, are

332 conducted.

333 Otherwise, this invertebrate phylum is the most successful and abundant in the globe, dominating soil, water

334 and air. Learning ways to add them to food platter can be a significant solution in the face of the 'food dearth'. Also,

335 this present 'taboo' is judged to be more nutritious and less toxic than many of current market foods, replete with

336 chemicals additives, antibiotics and hormones. For example, synthetic food dyes prevalent in processed food are

337 made from coal tar sludges. Attention deficit hyperactivity disorder (ADHD) in children has been consistently linked

338 to these artificial dyes in foods (Rippere, 1983).

339 Suggesting novel foods, based on arthropods/edible insects, might be an interesting area in food development.

340 Generalization does not hold true in any science concept. Similarly, arthropods might not be entirely unsuitable or

341 suitable for food. May be not all, but certainly some insects are worth incorporating into food, as proven by a myriad

342 studies. Their processing routes and the dosage consumed are important determinants in this regard. 343 Ultimately, just like personal choices of non-vegetarian,MANUSCRIPT vegan or vegetarian mode of eating, the adoption of 344 entomophagy depends on the consumer. When it comes to food, like religion, the views are fiercely guarded. The 345 same individuals, who relish shrimps, doling out a large sum on these foods, can be averse at the thought of eating

346 crickets. Some cultures dislike mushrooms, while others enjoy penicillium-fermented blue cheese. Some people

347 enjoy the tripe, and snouts of animals, while others shiver at the mention of it. Expecting everybody to eat insect-

348 based food is naive. But in the impoverished region with food shortage, encouraging the farming of edible insects

349 can be life-saving, and economy-boosting. Farming of the arthropods especially edible insects are easy for their high

350 fecundity, and less required space. The high turn-over rate and the maximum utilization of space renders ‘food-grade

351 edible insects rearing’ a lucrative option.

352 Perception of the Western World towards this dietary choice should not matter much, as they are not facing

353 the same constraintsACCEPTED of food insecurity. Of course, the entomophagous groups ought to be educated regarding the

354 risks of handling allergeniferous and pathogen-transmitting arthropods. To gather more epidemiological data of the

355 ill-effects of arthropod consumption, additional surveys, case studies and cohort assessments ought to be conducted.

356 Funding bodies are providing funds to research on this aspect. In coming times, significant improvement in the usage

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357 of the arthropods especially edible insects as alternative nutrition source is expected to escalate. In this arrangement,

358 everybody wins, and environmental balance can be restored.

359 Conclusions

360 ‘An individual’s perception of bizarre food is nutritious delicacy for another individual’. Edible insects

361 symbolize this truth. For thousands of years, mankind has derived nourishment from these critters. They hold

362 enormous potential to be developed as food. However, safety evaluations are needed. If researchers find ample

363 nutritional benefits, with negligible risks, overcoming the feeling of ‘disgust’ will not be difficult. This review is

364 likely to be a groundwork for that vision.

365 Declaration

366 There is no conflict of interest in submission of this manuscript.

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ACCEPTED MANUSCRIPT Table 1. Arthropod orders Species

Coleoptera Beetle larvae and pupae

Hemiptera Giant water bugs and cicadas

Hymenoptera Ants and bees

Isoptera Termites

Lepidoptera Moth and butterfly larvae and pupae

Orthoptera Cricket, grasshoppers, and locusts

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Fig. 2

Arthropods Protein Serineproteases Omega-3 fats Grasshoppers, Aspartic protease crickets, ants, Calcium Calycin Iron locusts, cicadas, Tropomyocin scale insects, Selenium Chitin Zinc beetles, weevils, termites, flies Vitamin B Asthma Dermatitis Sinusitis Rhinitis Hunger Otitis Malnutrition Anaphylaxis

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• The World is facing food insecurity and it requires prospecting of underutilized nutritious foods. • Arthropods, with abundance of proteins, unsaturated fats and minerals are potent candidates. • However, the allergens, status as pathogen vectors and ‘disgust factors’ undermine their food candidature. • This review analyzes the pros, cons and scopes of entomophagy.

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